Wheat Transcriptional Corepressor TaTPR1 Suppresses Susceptibility Genes TaDND1/2 and Potentiates Post-Penetration Resistance against Blumeria graminis forma specialis tritici.

The obligate biotrophic fungal pathogen Blumeria graminis forma specialis tritici (B.g. tritici) is the causal agent of wheat powdery mildew disease. The TOPLESS-related 1 (TPR1) corepressor regulates plant immunity, but its role in regulating wheat resistance against powdery mildew remains to be disclosed. Herein, TaTPR1 was identified as a positive regulator of wheat post-penetration resistance against powdery mildew disease. The transient overexpression of TaTPR1.1 or TaTPR1.2 confers wheat post-penetration resistance powdery mildew, while the silencing of TaTPR1.1 and TaTPR1.2 results in an enhanced wheat susceptibility to B.g. tritici. Furthermore, Defense no Death 1 (TaDND1) and Defense no Death 2 (TaDND2) were identified as wheat susceptibility (S) genes facilitating a B.g. tritici infection. The overexpression of TaDND1 and TaDND2 leads to an enhanced wheat susceptibility to B.g. tritici, while the silencing of wheat TaDND1 and TaDND2 leads to a compromised susceptibility to powdery mildew. In addition, we demonstrated that the expression of TaDND1 and TaDND2 is negatively regulated by the wheat transcriptional corepressor TaTPR1. Collectively, these results implicate that TaTPR1 positively regulates wheat post-penetration resistance against powdery mildew probably via suppressing the S genes TaDND1 and TaDND2.

Priming seeds for the future: Plant immune memory and application in crop protection.

Plants have evolved adaptive strategies to cope with pathogen infections that seriously threaten plant viability and crop productivity. Upon the perception of invading pathogens, the plant immune system is primed, establishing an immune memory that allows primed plants to respond more efficiently to the upcoming pathogen attacks. Physiological, transcriptional, metabolic, and epigenetic changes are induced during defense priming, which is essential to the establishment and maintenance of plant immune memory. As an environmental-friendly technique in crop protection, seed priming could effectively induce plant immune memory. In this review, we highlighted the recent advances in the establishment and maintenance mechanisms of plant defense priming and the immune memory associated, and discussed strategies and challenges in exploiting seed priming on crops to enhance disease resistance.

Exploiting Epigenetic Variations for Crop Disease Resistance Improvement.

Pathogen infections seriously threaten plant health and global crop production. Epigenetic processes such as DNA methylation, histone post-translational modifications, chromatin assembly and remodeling play important roles in transcriptional regulation of plant defense responses and could provide a new direction to drive breeding strategies for crop disease resistance improvement. Although past decades have seen unprecedented proceedings in understanding the epigenetic mechanism of plant defense response, most of these advances were derived from studies in model plants like Arabidopsis. In this review, we highlighted the recent epigenetic studies on crop-pathogen interactions and discussed the potentials, challenges, and strategies in exploiting epigenetic variations for crop disease resistance improvement.

Origins and Evolution of Cuticle Biosynthetic Machinery in Land Plants.

The aerial epidermis of land plants is covered with a hydrophobic cuticle that protects the plant against environmental stresses. Although the mechanisms of cuticle biosynthesis have been extensively studied in model plants, particularly in seed plants, the origins and evolution of cuticle biosynthesis are not well understood. In this study, we performed a comparative genomic analysis of core components that mediate cuticle biosynthesis and characterized the chemical compositions and physiological parameters of cuticles from a broad set of embryophytes. Phylogenomic analysis revealed that the cuticle biosynthetic machinery originated in the last common ancestor of embryophytes. Coexpansion and coordinated expression are evident in core genes involved in the biosynthesis of two major cuticle components: the polymer cutin and cuticular waxes. Multispecies analyses of cuticle chemistry and physiology further revealed higher loads of both cutin and cuticular waxes in seed plants than in bryophytes as well as greater proportions of dihydroxy and trihydroxy acids, dicarboxylic acids, very-long-chain alkanes, and >C28 lipophilic compounds. This can be associated with land colonization and the formation of cuticles with enhanced hydrophobicity and moisture retention capacity. These findings provide insights into the evolution of plant cuticle biosynthetic mechanisms.

Update on Cuticular Wax Biosynthesis and Its Roles in Plant Disease Resistance.

The aerial surface of higher plants is covered by a hydrophobic layer of cuticular waxes to protect plant tissues against enormous environmental challenges including the infection of various pathogens. As the first contact site between plants and pathogens, the layer of cuticular waxes could function as a plant physical barrier that limits the entry of pathogens, acts as a reservoir of signals to trigger plant defense responses, and even gives cues exploited by pathogens to initiate their infection processes. Past decades have seen unprecedented proceedings in understanding the molecular mechanisms underlying the biosynthesis of plant cuticular waxes and their functions regulating plant-pathogen interactions. In this review, we summarized the recent progress in the molecular biology of cuticular wax biosynthesis and highlighted its multiple roles in plant disease resistance against bacterial, fungal, and insect pathogens.

Epigenetic Activation of Enoyl-CoA Reductase By An Acetyltransferase Complex Triggers Wheat Wax Biosynthesis.

The epidermal surface of bread wheat (Triticum aestivum) is coated with a hydrophobic cuticular wax layer that protects plant tissues against environmental stresses. However, the regulatory mechanism of cuticular wax biosynthesis remains to be uncovered in bread wheat. Here, we identified wheat Enoyl-CoA Reductase (TaECR) as a core component responsible for biosynthesis of wheat cuticular wax. Silencing of TaECR in bread wheat resulted in a reduced cuticular wax load and attenuated conidia germination of the adapted fungal pathogen powdery mildew (Blumeria graminis f.sp. tritici). Furthermore, we established that TaECR genes are direct targets of TaECR promoter-binding MYB transcription factor1 (TaEPBM1), which could interact with the adapter protein Alteration/Deficiency in Activation2 (TaADA2) and recruit the histone acetyltransferase General Control Nonderepressible5 (TaGCN5) to TaECR promoters. Most importantly, we demonstrated that the TaEPBM1-TaADA2-TaGCN5 ternary protein complex activates TaECR transcription by potentiating histone acetylation and enhancing RNA polymerase II enrichment at TaECR genes, thereby contributing to the wheat cuticular wax biosynthesis. Finally, we identified very-long-chain aldehydes as the wax signals provided by the TaECR-TaEPBM1-TaADA2-TaGCN5 circuit for triggering B graminis f.sp. tritici conidia germination. These results demonstrate that specific transcription factors recruit the TaADA2-TaGCN5 histone acetyltransferase complex to epigenetically regulate biosynthesis of wheat cuticular wax, which is required for triggering germination of the adapted powdery mildew pathogen.

Histone Deacetylase TaHDT701 Functions in TaHDA6-TaHOS15 Complex to Regulate Wheat Defense Responses to Blumeria graminis f.sp. tritici.

Powdery mildew disease caused by Blumeria graminis f.sp. tritici (Bgt) leads to severe economic losses in bread wheat (Triticum aestivum L.). To date, only a few epigenetic modulators have been revealed to regulate wheat powdery mildew resistance. In this study, the histone deacetylase 2 (HD2) type histone deacetylase TaHDT701 was identified as a negative regulator of wheat defense responses to Bgt. Using multiple approaches, we demonstrated that TaHDT701 associates with the RPD3 type histone deacetylase TaHDA6 and the WD40-repeat protein TaHOS15 to constitute a histone deacetylase complex, in which TaHDT701 could stabilize the TaHDA6-TaHOS15 association. Furthermore, knockdown of TaHDT701, TaHDA6, and TaHOS15 resulted in enhanced wheat powdery mildew resistance, suggesting that the TaHDT701-TaHDA6-TaHOS15 histone deacetylase complex negatively regulates wheat defense responses to Bgt. Moreover, chromatin immunoprecipitation assays revealed that TaHDT701 could function in concert with TaHOS15 to recruit TaHDA6 to the promoters of defense-related genes such as TaPR1, TaPR2, TaPR5, and TaWRKY45. In addition, silencing of TaHDT701, TaHDA6, and TaHOS15 resulted in the up-regulation of TaPR1, TaPR2, TaPR5, and TaWRKY45 accompanied with increased histone acetylation and methylation, as well as reduced nucleosome occupancy, at their promoters, suggesting that the TaHDT701-TaHDA6-TaHOS15 histone deacetylase complex suppresses wheat powdery mildew resistance by modulating chromatin state at defense-related genes.

Wheat WD40-repeat protein TaHOS15 functions in a histone deacetylase complex to fine-tune defense responses to Blumeria graminis f.sp. tritici.

Powdery mildew caused by Blumeria graminis f.sp. tritici (Bgt) seriously threatens the production of common wheat (Triticum aestivum). In eukaryotes, WD40-repeat (WDR) proteins usually participate in assembling protein complexes involved in a wide range of cellular processes, including defense responses. However, the potential function of WDR proteins in regulating crop resistance to biotrophic fungal pathogens, such as Bgt, remains unclear. In this study, we isolated TaHOS15, encoding a WDR protein, from the Bgt-susceptible wheat cultivar Jing411 and demonstrated that knockdown of TaHOS15 expression using virus- or transient-induced gene-silencing attenuated wheat susceptibility to Bgt. Biochemical and molecular-biological assays revealed that TaHOS15 interacts with TaHDA6, a wheat homolog of Arabidopsis histone deacetylase AtHDA6, to constitute a transcriptional repressor complex. We determined the role of TaHOS15, which might act as an adaptor protein recruiting TaHDA6 to the chromatin of wheat defense-related genes including TaPR1, TaPR2, TaPR5, and TaWRKY45, where they repress histone acetylation. Reduced TaHOS15 or TaHDA6 transcript levels led to decreased susceptibility to Bgt together with enhanced defense-related transcription under Bgt infection. Collectively, these results demonstrate that TaHOS15 functions in a histone deacetylase complex with TaHDA6 to fine-tune the defense response to Bgt in common wheat.

Wheat CHD3 protein TaCHR729 regulates the cuticular wax biosynthesis required for stimulating germination of Blumeria graminis f.sp. tritici.

Powdery mildew caused by Blumeria graminis f.sp. tritici (Bgt) is a detrimental disease of bread wheat (Triticum aestivum). Bgt infection initiates with the germination of its conidia, which is stimulated by plant cuticle-derived wax signals. Here, we identified wheat 3-KETOACYL-CoA SYNTHASE (TaKCS6), a homolog of barley HvKCS6, as a key enzyme in the biosynthesis of wheat cuticular wax. We found that both cuticular wax accumulation and Bgt germination were impeded on leaves of TaKCS6-knockdown plants. The TaKCS6 promoter-associated bHLH type transcription factor 1 (TaKPAB1) binds to the TaKCS6 promoters and recruits the CHD3 protein TaCHR729 to them via physical association. Knockdown of TaCHR729 results in decreased trimethylation of histone H3 Lys 4 (H3K4me3) at the TaKCS6 promoters and down-regulation of TaKCS6 transcription, leading to a reduction of cuticular wax accumulation and Bgt germination on leaves. We further identified very-long-chain aldehydes with a chain length above C24 as the signals regulated by the TaCHR729-TaKPAB1-TaKCS6 pathway for stimulating Bgt germination. Our study thus reveals that the transcription factor-mediated recruitment of chromatin remodeling machinery is essential for regulating the biosynthesis of cuticular wax that is required for stimulating Bgt germination in bread wheat.